Limnol. Oceanogc, 35(2), 1990,28?-295
Q 1990, by the American Society of Limology
and Oceano~raplty,
Inc
Lead in marine planktonic organisms and pelagic food webs
Anthony F. Michaels’
Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543
A. Russell Flegal
Institute of Marine Sciences, University of California, Santa Cruz, Santa Cruz 95064
Abstract
The bioaccumulation of lead in biological ecosystems traditionally has been interpreted in terms
of the atomic ratio of Pb to Ca. In marine planktonic ecosystems, however, most of the particulate
Ca is skeletal and its amount variable among taxa. The Pb in plankton can be partitioned between
skeletal and nonskeletal components. In planktonic samples collected in the equatorial Pacific
Ocean, ~0.5% of the Pb was associated with CaCO, (primarily foraminiferan, coccolithophorid,
and pteropod skeletons), while up to 54k of the Pb in these samples may have been associated
with the SrSO, skeletons and protoplasm of Acantharia. Atomic ratios of Pb to Ca were highly
variable, principally because of the varying amounts of CaCO, in the samples. Therefore, normalizing Pb concentrations to biomass rather than Ca is preferable for interpreting the bioactivity
of Pb in planktonic food webs. We develop a simple model based on the ratio of surface area to
volume of organisms to make predictions about the relative importance of organism size and foodweb interactions in the transfer of Pb between trophic levels. For small organisms (<270-pm
spherical radius or the equivalent surface: volume ratio), Pb concentration is determined almost
entirely by surface area. For larger organisms, total body Pb will be a function of both the size of
the prey and the distribution of Pb within tissues. The role of food-web interactions (e.g. grazing)
in determining the amount of Pb in plankton of different sizes will only be important for large
plankton and nekton, where very little of it is adsorbed on the animal surface.
Terrestrial ecosystems are characterized
by sequential decreases in the atomic ratio
of Pb to Ca at successive trophic levels (Elias
et al. 1976). This pattern parallels the distribution of Sr, which is also cycled as a
biochemical analog of Ca in terrestrial ecosystems (Comar 1965). More than 90% of
the Pb in vertebrates is concentrated in calcareous skeletal material, and Pb toxicity is
associated with the alteration of Ca-mediated, cellular processes and the mimicry
of Ca in binding to regulatory proteins (N&l.
Acad. Sci. 1980). The atomic ratio of Pb to
I New address: Bermuda Biological Station for Research, Inc., 17 Biological Station Lane, Ferry Reach,
GE 0 1 Bermuda.
Acknowledgments
We thank C. Patterson for providing lab facilities
for data analysis and critical discussion of the data, K.
Buesseler, S. Fowler, and M. Silver for discussions of
the model, and V. Fabry, N. Fisher, S. Fowler, L. Madin, K. Orians, and L. Small for reviews of the manuscript.
This research was supported in part by an NSF grant
(OCE 86-12113) to A.R.F.
Woods Hole Oceanographic Institution Contribution 6988.
287
Ca systematically decreases at each trophic
level (termed biopurification)
because Ca is
selectively transported across cell membranes, preferentially retained in metabolic
processes, and preferentially removed in detoxifying processes.
A review of the transport of trace metals
in marine food chains (Bernhard and Andreae 1984) reiterates Burnett and Patterson’s (1980) proposal that there is a similar
systematic reduction in the relative concentration of Pb in marine ecosystems. It indicated that Pb concentrations
increase
about 100,000 times from seawater to the
first trophic level and then decrease in higher
trophic levels. That proposal was based on
a very limited number of measurements
(Burnett and Patterson 1980; Settle and Patterson 1980) of Pb concentrations in seawater, an intertidal macroalga (Vulonia ventricosa), an intertidal
mussel (Mytilus
crustacean
californianus), an intertidal
(Panulirus interruptus), and a pelagic fish
(Thunnus alalmga). Most other published
concentrations of Pb in marine organisms
are considered invalid (Bernhard and Andreae 1984). Therefore the intertidal macro-
288
Michaels and Flegal
alga (IT ventricosa) and the crustacean (J’.
interruptus) were used as analogs of phytoplankton and zooplankton to develop a
hypothetical model for the systematic reduction in atomic ratios of Pb to Ca in pelagic food webs that paralleled terrestrial
models (Burnett and Patterson 1980).
Subsequent measurements of Pb concentrations in pelagic organisms have partially
disproved those models (Flegal 1985; Flegal
and Patterson in prep., this paper). These
measurements substantiate the sequential
decrease in the atomic ratios of Pb to Ca
with increasing trophic levels in marine
nekton (e.g. fish), but there is not a corresponding decrease in the atomic ratios of
Pb to Ca in planktonic organisms. Atomic
ratios of Pb to Ca in plankton do not decrease systematica.lly because the ratio of Ca
to biomass varies substantially among phytoplankton and zooplankton taxa. Most Ca
is present in the skeletons of a small subset
of species: foraminiferans,
coccolithophorids:, and pelagic gastropods, while a substantial amount of the Pb in plankton probably is associated with organic tissue.
Therefore, atomic ratios of Pb to Ca in assem-blages of marine plankton reflect the relative predominance of calcareous and noncalcareous species, rather than the trophic
levels of those organisms.
The bioaccumulation
of Pb in marine
phytoplankton is dominated by surface uptake (Fisher et al. 1987). It includes adsorption, precipitation,
absorption, and other
physical, chemical, and biological processes
(Sposito 1986). Consequently, the concentration of Pb in marine phytoplankton
appears to be proportional to ~their ratios of
surface area to volume. Studies with phytoplankton cultures indicate that the bioaccumulation of Pb is relatively nonspecific
and invariant with physiological condition,
including death (Fisher et al. 1983, 1987).
Furthermore, Pb (a nonessential element)
has a. limiting-nutrient
type of distribution
in the ocean (Flegal and Patterson 1983). In
this respect it resembles the vertical distribution of particle-reactive transuranics (Am,
Pu, Cm) .that appear to have the same number of binding sites per unit of surface area
on diverse biological surfaces (Fisher and
Fowler 1987). Biological scavenging of Pb
is also indicated by the highly significant
correlations between the scavenging of 210Pb
by suspended particles and the particulate
organic C flux in seawater (Bacon et al. 198 5;
Moore and Dymond 1988), the relationship
between 210Pb fluxes and new production
(Fisher et al. 1989), and the correspondingly
short (54 yr) scavenging residence time of
stable Pb in ,the oceans (Craig et al. 1973).
The following analysis of processes a:ffecting the bioaccumulation
and biopurification of Pb in marine pelagic food webs
consists of two components. First, the partitioning of Pb between skeletal and organic
phases and the utility of Pb: Ca ratios in
planktonic samples is addressed with a limited number of ultra-clean measurements of
Pb, Sr, and Ca concentrations in marine
plankton. A more detailed analysis of the
elemental composition
of these plankton
samples will be published elsewhere @legal
and Patterson in prep.). Second, a simple
model is presented to predict the Pb concentration of marine plankton based on their
ratio of surface area to volume. Based on
the model results, we make first-order predictions of the behavior of Pb in pelagic
food webs and the relationship between the
flux of Pb from the euphotic zone and net
primary productivity.
Methods
Plankton samples-Plankton
data used in
the following analysis were collected and
analyzed with ultra-clean techniques comparable to those used for the corresponding
measurements of Pb concentrations in sea-,
water (Flegal and Patterson 1983) and marine nekton (Settle and Patterson 1980).
Sampling locations were in the equatorial
Pacific Ocean between 19’N and 15% and
150” and 158”W @legal 1985). Plankton
samples were collected in Nylon nets (64pm mesh) with conventional polyethylene
cod ends, attached to stainless steel bridles
(0.5-m diam) sealed in polyethylene. Surface water (l-l 0 m) tows. were made from
a raft after it had been rowed hundreds of
meters upwind and upcurrent from the re(operationsearch vessel. “Zooplankton”
ally defined as positively phototactic, motile
organisms and positively buoyant organ-
Pb in marine plankton
isms) were decanted after “phytoplankton”
settled out in an upright cod end within a
trace-metal-clean chamber aboard ship. The
two subsamples were filtered, frozen in acidcleaned polyethylene bottles, and vacuum
dried. Obvious zooplankton
(principally
Crustacea) were then picked from the phytoplankton samples before digestions for elemental analyses. In reality, both subsamples contained mixtures of phytoplankton
and zooplankton.
Elemental concentrations were measured
by isotope-dilution thermal-ionization
mass
spectrometry, following acid digestions and
dithizone extractions developed for seawater analyses (Flegal and Patterson 1983).
All sampling and analytical materials were
sequentially cleaned for several weeks with
trace-metal-clean
(two times subboiling
quartz-distilled) solutions of water and acids.
These preparations and subsequent analyses were conducted in a Class-100 laboratory. All sampling materials were stored in
acid-cleaned polyethylene bags within two
other polyethylene bags. The sum of contaminant Pb contributed from materials and
reagents used in sampling, storage, and
analysis was < 150 pg per sample. It accounted for < 1% of the Pb in each sample
aliquot.
Surface : volume models- The first model
for the amount of Pb in planktonic organisms is based on changes in the ratio of surface area to volume (S: V) with changes in
size. The dry weight-specific Pb concentration is calculated as
Pb (pg pg- ’ dry wt)
= (V F’bli + S F’b13. c1J
VD
V and S are the volume and surface area of
the organism, [Pb], is the internal concentration of Pb (pg pm-3), [Pb], the amount
of adsorbed Pb (pg pm-2), and D the conversion factor to dry weight from volume.
Values for both internal and external Pb
concentrations were estimated from published data for the alga V. ventricosa (Burnett and Patterson 1980) and from the 210Pb
concentration factors of phytoplankton cultures (Fisher et al. 1987). A dissolved Pb
concentration of 15 ng kg-’ was assumed
289
for the calculation of weight-specific
Pb
content from the concentration
factors.
From these data, the surface sorption of Pb
was set at 2 x 1Od6pg yrnm2 and the internal
Pb concentration at 2.5 X 10m9 pg prnd3.
For the first case of the model, both are held
constant for all sizes of organisms. D is constant at 0.24 (assuming vol/wet wt = 1.2,
dry wt/wet wt = 0.2, Valiela 1984). The total
weight-specific Pb values are converted to
units of pg g-r dry wt (+ 1,OOO,OOO).Total
Pb concentrations are predicted over the
range of S : Vratios in the marine biosphere,
from bacteria to fish.
Organisms will deviate from the predicted values in case 1 for many reasons, including biochemical processes that decrease
intracellular atomic ratios of Pb to Ca and
physiological processes that exclude Pb from
entering cells during digestion. These effects
are indicated by the inverse correlation between total Pb concentrations (pg Pb g-’ dry
wt) and body size in large terrestrial organisms (Elias et al. 1976) and marine pelagic
metazoans (Settle and Patterson 1980). Additionally, the fecal wastes of some marine
zooplankton are three times enriched in Pb
compared with their particulate food and
1O-20 times compared with the zooplankter
itself (Fowler 1977), demonstrating the relative mobility of organic biomass compared
with Pb in ingested food.
This size-based biopurification
is incorporated in the second case of the model,
which decreases the internal Pb concentration by a factor of 10 with each order of
magnitude increase in the equivalent spherical radius in the larger organisms. Here,
larger organisms are defined as those with
a S : V ratio of CO. 1 pm2 pm-3 (equal to a
sphere of 30-pm radius). Thus for organisms with S: V -=z0.1,
Pblic~30j= IPWi~~30~
(304
is
the
internal
Pb
concentration
Pbli(c30)
(2)
for
organisms of < 30-ym equivalent spherical
radius (ESR, S: V >O.l pm2 pmm3) and r
the ESR for each S: V ratio. Changes in
internal Pb content that result from this
modification are comparable to published
values of the decrease in Pb with size among
pelagic metazoans (Settle and Patterson
1980).
290
Michaels and Flegal
Talble 1. Dissolved lead ([Pb],i,) (pg g-l) and planktonic Pb (gg g-l), Sr (mg g-l), and Ca (mg g-1) concentrations from the central Pacific Ocean.
-ST
Sta.
Sample type
Pb
ca
IF%
-1
13.0 Mixed plankton
2.4 250.0 32.0
5.6 Zooplankton
7.4
31
37
4.3 Phytoplankton
0.76
2::: 2z.z
Zooplankton
0.72
5.9
I:6
44
5.6 Phytoplankton
51.0 21.0
0.77
Zooplankton
3.3
0.0 0.0
69
5.3 Phytoplankton
0.62
0.0 48.0
Zooplankton
7.2 16.0
0.41
84
5.5 Phytoplankton
1.8
60.0 35.0
Zooplankton
16.0 17.0
0.16
Ichthyoplankton
0.15
1.6 3.5
9s
4.2 Phytoplankton
0.53
15.0 53.0
Zooplankton
1.9
10.0 13.0
--
Results
TotalPbconcentrations inplankton--Total Pb concentrations &g g-l dry wt) of the
plan.kton samples range from 0.15 to 7.4 pg
g-i dry wt (Table 1). These concentrations
are similar to those obtained by Martin and
Knauer (1973) and substantially lower than
most other published reports of Pb concentrations in marine plankton. The Ca and Sr
concentrations are within the normal range
of concentrations
in net samples of marine
plankton (Martin and Knauer 197 3; Collier
and Edmond 1984).
The total Pb coacentrations include the
Pb sorbed on cell surfaces, within organic
tissues, and associ.ated with various inorganic carrier phases. The latter include calcium carbonate (CaCO,) and celestite
(SrSO,) skeletons. The following calculations; provide prehminary estimates of the
partitioning of the Pb between those skeletal
and organic phases.
Estimates of the partitionirzg of Pb within
the plankton -The fractions of planktonic
Pb associated with two of the principal skeletal types, CaCO, and SrS04, were estimated with distribution coefficients (&) for
Pb in these skeletons. Calcium carbonate
skeletons are found in coccolithophorids
(unicellular and colonial algae), foraminiferans (sarcodine protozoans), and pteropods (pelagic gastropods). Acantharia (sarcodine protozoans) make a celestite skeleton
and ,account for most of the particulate Sr
in the plankton (e.g. Bishop et al. 1977). A
Table 2. Estimates of the partitioning of Pb into
two operationally defined groups ol skeleton-bearing
organisms.
Percent of Pb in
SIFI.
7
31
37
44
69
84
95
Sample type
Mixed plankton
Zooplankton
Phytoplankton
Zooplankton
Phytoplankton
Zooplankion
Phytoplankton
Zooplankton
Phytoplankton
Zooplankton
Ichthyoplnnkton
Phytoplankton
Zooplankton
srso,
53.5
0.1
6.5
2.0
14.6
0.0
0.0
3.7
7.2
21.7
2.3
4.7
0.9
-.
taco,
0.1
0.4
0.14
czo.01
0.1
0.0
0.24
0.11
0.1
0.34
0.1
0.24
0.02
remainder
46.4 99.5
93.4
98.0
85.3
100.0
99.8
96.2
92.7
78.0
97.6
95.1
99.1
Kd for Pb in CaCO, of 2.3 was reported for
the CaCO, tests of corals (Shen and Boyle
1987) and is used here. The tests of COG
colithophorids,
foraminiferans,
and ptero-,
pods may contain different proportions of
Pb than corals, but the present analysis is
relatively insensitive to the absolute value
of this distribution
coefhcient. The Pb: Sr
molar ratio in Acantharia from three locations in the Southern California Bight averaged 3.5 x 1Oe5 (Michaels and Coale in
prep.), and the lowest value was 7 .O x 1Oe6.
At a surface Pb concentration of 15 ng kg-‘,
the low Acantharia value indicates a & of
3.0. In the samples analyzed by Michaels
and Coale (in prep.), Pb in the skeleton cannot be unambiguously distinguished from
Pb associated with the tissues; thus this iYd
represents the Pb associated with Acantharia as a group and not just with their
skeletons. (Both the methods used to analyze the samples and the relatively low concentrations of Pb in tissues suggest that much
of this Pb is in the skeleton, Coale pers.
comm.) These distribution coefficients were
used to estimate the amount of Pb associated with CaCO, skeletons and the skeleton
and body of acantharians. The analysis indicates that calcareous skeletons uniformly
account for ~0.5% of the Pb within the
plankton samples (Table 2), while Acantharia appear to account for O-54% of the
Pb.
In samples that were divided into phytoplankton (sinking organisms) and zoo-
Pb in marine plankton
plankton (swimming or floating organisms)
subsamples, the phytoplankton subsample
usually contained more Ca (Table 1) and
had a larger fraction of the Pb associated
with calcareous skeletons (Table 2). The
major exception is station 84, where there
is a small amount of Pb and a relatively
large amount of Ca in the zooplankton sample. The amount of particulate Sr in these
samples is also variable, and in most samples Sr is more prevalent in the phytoplankton subsamples (Table 1).
Acantharia, with their celestite skeletons,
seemto be significant carriers for Pb in communities of the larger plankton (Table 2).
For these estimates, we used a conservative
& for Pb in Acantharia (skeleton and tissue
combined). At station 7, Sr was 25% of the
sample by weight and SrSO, would be 53%
of the sample weight. The weight of organic
C in acantharians from the North Pacific
was 87% of the Sr weight (Michaels unpubl.
data). Thus, - 74% by weight of the sample
at station 7 was acantharians. These calculations indicate that Acantharia contained at least 54% of the Pb in this sample,
which suggeststhat the Pb : Sr ratio reported
by Michaels and Coale (in prep.) and the
tentative Kd used in this paper are appropriate.
The Pb associated with other materials,
including organic matter, is estimated to
range from 46 to 100% of the total Pb content of the samples (Table 2). In the paired
samples, the median amount of Pb associated with the phytoplankton fractions is 0.76
bg g-i and the median associated with zooplankton is 0.72 [phytoplankton mean (SD)
= 0.90(0.52), zooplankton
mean =
1.30(1.30) pg g-l]. Despite the similarity in
weight-specific Pb content of phytoplankton and zooplankton subsamples, the median Pb : Ca ratio of the zooplankton subsampIes is 5.6 times higher than that of the
phytoplankton subsamples. This apparent
Pb enrichment is due more to the differences in the Ca content of the subsamples
than to differences in the Pb content.
Surface: volume model-Model Pb concentrations for case 1 ,(constant internal Pb
concentration) are highest for the smallest
organisms and show a linear decreasewith
increasing size (Fig. 1). For organisms of
291
Equivalent
3
0.001
’
Spherical
0.01
’
0.1
’
Radius (mm)
1.0
’
10.0
’
1wx
’
l
-4;
10.0
,
1.0
,
0.1
1
0.01
,
0.001
(
O.WOl 0.
091
Surface : Volume Ratio (l/m)
Fig. 1. Predicted and measured Pb concentrations
in plankton. The two lines are the predicted Pb concentrations with size from the S : V model. The solid
line is for case 1-constant internal Pb concentrations.
The dashed line is for case 2--variable internal Pb
concentrations in larger grazers. The symbols are measurements of Pb concentrations in plankton and nekton
from published values. Concentration factors for *‘“Pb
were converted to total Pb assuming 15 ng Pb liter-r.
S: V ratios were estimated from the shape of the organism or the mesh size of the plankton nets used to
collect the samples. 0-Phytoplankton
samples from
coastal California (from A. R. Flegal et al. in prep.);
a-algal cultures (from Fisher et al. 1987); O-zooplankton (from Fowler 1977); n -zooplankton and
nekton (from Heyraud and Cherry 1979); A-zooplankton (from Martin and Knauer 1973): A-marine
fish (from‘Patterson and Settle 1977, tuna; Settle and
Patterson 1980, anchovy; Flegal and Patterson in prep.,
white croaker and english sole).
<300-pm equivalent spherical radius (ESR),
nearly all of the Pb is adsorbed to the cell
surface. At > IO-mm ESR, Pb concentrations become constant at the internal Pb
concentration, with surface Pb accounting
for < 1% of total content. Therefore, nearly
all of the Pb is bound to the surface for the
smallest organisms and is internal for the
largest organisms (Fig. 2).
The organisms are arbitrarily divided into
three size groups. The boundaries between
the groups are the S: V where 90% of the
Pb is in one of the two areas (surface or
internal). At the size where 90% of the Pb
is either on the surface or internal, an orderof-magnitude change in the concentration
of Pb in the smaller component (10%) will
result in only a factor of two change in the
total Pb content of the organism. Type 1
292
Michaels and Flegal
Equivalent Spherical Radius (mm)
0.001
loo
0.01
0.1
1.0
100.0
10.0
I
7
---7
Surface /
80 4
r
B
Et
40-
$
1
20 -
I
,I--
Id.0
Internal ,
1:o
3
2
0:i
)/:
~
/
y--.
.
Oil
0.601
O.Obol
ox
Surface : Volume Ratio (l/m)
Fig. 2. Predicted partitioning of Pb between the
organism surface and the internal body based on case
1 of the 5’: V model.
organisms have most of their Pb (> 90%)
sorbed on the surface, and relatively large
changes in the internal Pb concentration
have little impact on their total Pb contents.
Conversely, type 3 organisms have most of
their Pb (> 90%) within their body and relative:ly large changes in the amount of Pb
sorbe:d on their surfaces will have negligible
changes in their total Pb contents. Type 2
organisms are intermediate, and both Pb
sorption on their surfaces and internal Pb
concentrations are important.
Biopurification
changes the predicted Pb
concentrations for the larger organisms (case
2). We only applied the biopurification
rule
to larger organisms (types 2 and 3), where
metabolic changes in the internal concentration of Pb may substantially change the
total Pb content (.st?eabove). Pb concentrations in this second case decline with increasing size over the entire size range (Fig.
1, dashed line). The pattern in type 1 organisms is caused by the S : V relationship;
the pattern in the other two size classes is
cause:d primarily by biopurification. For case
2, gnazing-based biopurification
results in
an order-of-magnitude
less Pb for each order-of-magnitude increase in size. Changing
this ratio will change the slope of the predicted line for the larger organisms.
Discussion
Partitioning of Pb in the marine biosphere--Atomic
ratios of Pb to Ca have pro-
vided insights into the biogeochemical cycle
of the element and its movement between
trophic levels in vertebrate food webs.
However, as illustrated here, the relationship breaks down in the lower levels of pelagic food webs, where the mass of calcareous structures is extremely variable. Most
of the particulate Ca in marine plankton is
in the skeletons of foraminiferans
(protozoans), coccolithophorids
(unicellular and
colonial algae), and pteropods (pelagic gastropods). Each group of these organisms
covers a large size range: foraminiferans, 202,000 pm; coccolithophores,
~20 pm for
individuals and up to a few millimeters for
colonies; pteropods, < 1 10 - 10 mm. The
area1 distributions of these taxa are very heterogeneous on scales of meters to hundreds
of kilometers.
Consequently,
calcareous
skeletons will be variable components of
plankton samples (Martin and Knauer 1973;
this paper). Our analysis indicates that variation in the relative abundance of organisms with calcareous skeletons accounts for
most of the variation in Pb: Ca ratios in
mixed plankton samples.
The fate of Pb on sinking particles and
the relationship between Pb fluxes and organic C fluxes is affected by its distribution
among carrier phases. The sinking of large
particles has been identified as the primary
mechanism determining the vertical fluxes
of C (McCave 1975). Plankton nets, such as
those used in this study, sample this pool
of large organisms and particles. A small
fraction of the Pb is associated with CaCO,
skeletons. When coccolithophorids
or possibly foraminiferans and pteropods are very
abundant, this fraction may be larger. CaCO,
comprises a large fraction of the particulate
sinking material, especially near the seafloor, where carbonate fluxes can be >90%
of the total mass flux (Honjo 1982). This
change in the relative importance of carbonates is due to their relative insolubility
compared with organic material. Consequently, Pb in carbonates becomes a relatively more important component of the total Pb flux with depth.
Pb associated with sinking &-SO, will be
more labile. The oceans are undersaturated
with respect to SrSO,, which makes celestite
a very labile carrier phase for associated
metals like Pb (Bernstein et al. 1987; Mi-
Pb in marine plankton
chaels and Coale in prep.). The skeleton of
an acantharian dissolves rapidly after the
protozoan dies or is eaten, as evidenced by
the fivefold decrease in the celestite flux between 100 and 300 m in the North Pacific
(Michaels and Coale in prep.). This dissolution may contribute to the subsurface
maxima of dissolved Pb concentrations in
the oceans.
A simple surface area : volume modeiThe transfer of Pb and other adsorbed metals through planktonic food webs is determined by a variety of physical and biological properties. Seawater concentrations and
adsorption kinetics control the amount of
Pb that is present on biological surfaces (Davies 1983; Fisher et al. 1987; Jannasch et
al. 1988). The lability of surface-adsorbed
Pb, and to a lesser extent internal Pb, in
acidic digestive vacuoles or guts controls the
availability of adsorbed Pb to the consumer
(Davies 1983). In larger, more complex organisms, the amount and distribution of Pb
inside the prey animal and the lability of
the Pb in different body parts (e.g. bone vs..
muscle) will be important. Understanding
the relative importance of each of these effects is necessary for explaining the observed distributions
of trace elements, including Pb, in marine organisms.
We predict that the total concentration of
Pb in the three model-defined types of organisms will be influenced by different processes. Food-web interactions (herbivory
and carnivory) may lead to variations in the
internal Pb concentration of an organism.
Most marine organisms consume food particles that are at least 5-10 times smaller in
size. Our simple model predicts that these
prey organisms will generally have higher
total Pb concentrations than the predator
and may be expected to lead to changes in
the internal Pb concentration
of grazers
compared with nongrazing organisms such
as phytoplankton.
Feeding by animals in the type 1 size class
will not lead to changes in total Pb concentrations because the amount of surface-adsorbed Pb is great compared with internal
Pb concentrations. The type 1 category (0. l270-pm ESR) probably covers most of the
phytoplankton
and zooplankton
in the
oceans. These organisms (especially bacteria) also constitute most of the biological
293
surface area in the oceans (Cho and Azam
1988). Thus, food-web interactions among
the organisms responsible for most production, grazing, and remineralization
in the
euphotic zone and below are predicted to
be largely irrelevant in terms of the distribution of Pb among these organisms. Although biopurification
does occur in zooplankton in this size range, the changes in
the internal Pb concentration
likely are
overshadowed by the large amount of Pb
sorbed to their surfaces. The amount of
grazing on bacteria and other picoplankton
is probably less relevant to the geochemical
fluxes (particularly vertical fluxes) of Pb than
what kind of organism (large vs. small) does
the grazing.
Type 2 organisms will alter their total Pb
concentrations with changes in the amount
of internal Pb. These animals probably feed
on type 1 or smaller type 2 organisms, and
changes in their internal Pb concentration
probably are related to the size (total Pb) of
their prey. A salp which consumes nanoplankton (2.0-20.0~pm diam) may have a
higher internal Pb concentration than a copepod which consumes larger net phytoplankton. Salps do have elevated concentrations of 210Pb(Krishnaswami et al. 1985),
perhaps as a result of the small size and high
Pb content of their prey.
Type 3 organisms have a relatively insignificant fraction of their total Pb adsorbed
to their surfaces (< 1O%), and their total Pb
loads are dominated by their trophic interactions with prey. Their Pb concentrations
will be affected by the same size considerations as type 2 animals and may also be
affected by the structural complexity of their
prey. Many of the animal predators and prey
in this size range are fish. Fish sequester a
large fraction of their Pb in their bones (Patterson and. Settle 1977) which makes this
Pb relatively inaccessible to predators. At
the same time, the preferential placement
of Pb in bone reduces the concentration of
Pb in tissue compared to the total organismal Pb concentration. For both type 2 and
3 organisms, the nature of the digestive system (e.g. the presence of an acidic gut) is
likely to affect the mobility and incorporation of ingested Pb.
In summary, this model provides a simple and reasonable framework for inter-
Michaels and Flegal
prcting metal concentrations in planktonic
food webs. In case 1 of~this model we assume that the Pb : Sand Pb : Vrelationships
are constant for all organisms. However, the
adsorption kinetics and internal uptake
properties in organisms of very different
sizes may be variable. If the internal Pb
concentration of algae is due to passive uptake from the cell surface, large algal cells
may have lower internal Pb concentrations
than small cells becauseof their smaller S : I/
ratio. Adsorption rates onto radiolarian axopodia probably differ from those onto
crustacean cuticle. Cellular uptake of Pb
from the food vacuole of a protozoan may
differ from uptake in the gut of a tuna. These
details of the fate of Pb in ingested food
warrant further study, both as tests of the
assumptions of the model and for elucidating real biological processesthat are not included in this simple framework.
IComparison with measured data -Measured and calculated Pb concentrations in
marine plankton and nekton fit the model
predictions well, considering the wide range
of organism sizes and seawater Pb concentrations. Algal and cyanobacterial Pb levels
derived from *‘OPbconcentration factors in
urnalgal cultures (Fisher et al. 1987, closed
circles in Fig. 1) show a steeper slope with
S :: Vratio than the model predicts. This departure may be due to specific properties of
these species or reflect a size-based change
in Pb sorption onto algal surfaces. Animal
Pb levels are generally higher than the predictcd values (Fig. 1, squaresand triangles).
This deviation may be due to the increased
surface area in complex animals compared
with their nominal shapes (e.g. spheres,
avoids, etc.). Animals may also have higher
imernal (due to their diets) and external
(unique surface characteristics) Pb concentrations than algal cells. Although the larger
fish (closed triangles) fall on the case 1 line
(no biopurification), the relationship between the fish of different sizes has the same
slope as is predicted from biopurification.
‘I he scatter in the data may also reflect variations in the dissolved Pb concentration
among environments where the samples
were collected. Knowledge of dissolved Pb
cioncentrations (rarely measured in most
studies) is critical for accurate comparison
of different data sets, since concentration
factors are more readily comparable than
absolute concentrations (e.g. Fisher et al.
1987).
Food web and jlux
predictions-Food
webs of similar length and carbon flow are
predicted to have dramatically different
amounts of Pb passed to the higher trophic
levels, depending on the community structure. For example, a large diatom-crustacean-fish food web will lead to lower Pb
levels in the fish than a nanoplankton-salpfish food web that supports the same-sized
fish population. Large diatoms would have
relatively little adsorbed Pb, and, in Crustacca, much of the Pb is concentrated in the
indigestible exoskeleton (Fowler 1977). The
nanoplankton would have large amounts of
adsorbed Pb and the salp probably has most
of its Pb in easily digestible tissue. As previously mentioned, salps have a high internal Pb concentration (from 2’oPb)compared
with other marine organisms of the same
size (Krishnaswami et al. 1985).
Bacteria contain most of the biological
surface area in the ocean (Cho and Azam
.1988) and picoplankton have higher volume : volume concentration factors for surfacereactive metals than larger algae(Fisher
1985). Most of the Pb that enters the ocean
surface is probably adsorbed onto bacteria
and processedin the “microbial loop” where
a variable proportion of the microbial organic matter is ultimately converted to sinking particles. The sinking export of radionuclides (including 210Pb)is linked to the
rate of new production in the euphotic zone
(Fisher et al. 1989). Our model analysis suggests that much of the microbial activity
may be irrelevant for the ultimate export of
Pb from the upper ocean, presumably on
large, rapidly sinking particles. More important is the nature of the aggregation process that produces large particles (e.g. fecal
pellet and marine snow production and the
settling of algal blooms) and the extent to
which smaller particles are directly packaged into the large, sinking particles. The
inclusion of picoplankton directly into the
marine snow particle will lead to higher Pb
fluxes than the production of a fecal pellet
at the end of a longer grazing chain (e.g.
picoplankton-flagellate-ciliate-copepod),
Pb in marine plankton
even though the latter may include a larger
amount of picoplankton-produced
biomass.
295
ct al. [cds.], Oceanic processesin marine pollution.
2: Physico-chemical processes and wastes in the
ocean. Krieger.
-,
J.-L. TEYSSIE,S. KRISHNASWAMI,AND M. BASKARAN. 1987. Accumulation of Th, Pb, U, and
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